Causes and evolutionary significance of genetic convergence Pascal-Antoine Christin 1 , Daniel M. Weinreich 1 and Guillaume Besnard 2 1 Department of Ecology and Evolutionary Biology, Brown University, Providence, RI 02906, USA 2 Imperial College Silwood Park Campus, Buckhurst Road Ascot, Berkshire SL5 7PY, UK Convergent phenotypes provide extremely valuable sys- tems for studying the genetics of new adaptations. Accumulating studies on this topic have reported sur- prising cases of convergent evolution at the molecular level, ranging from gene families being recurrently recruited to identical amino acid replacements in distant lineages. Together, these different examples of genetic convergence suggest that molecular evolution is in some cases strongly constrained by a combination of limited genetic material suitable for new functions and a restricted number of substitutions that can confer specific enzymatic properties. We discuss approaches for gaining further insights into the causes of genetic convergence and their potential contribution to our un- derstanding of how the genetic background determines the evolvability of complex organismal traits. Evolutionary convergence provides outstanding study systems During the billions of years of evolution, similar selective pressures have occasionally led to the independent evol- ution of identical or similar traits in distantly related species, a phenomenon referred to as phenotypic conver- gence [1,2]. The recent wide use of genetic and/or phyloge- netic approaches has uncovered diverse examples of repeated evolution of adaptive traits including the multiple appearances of eyes [3,4], echolocation in bats and dolphins [5,6], pigmentation modifications in vertebrates [7–10], mimicry in butterflies for mutualistic interactions [11], convergence of some flower traits in plants [12–15], and multiple independent evolution of particular protein proper- ties [16,17]. The multiple origins of a trait represent excep- tional replicates of evolutionary processes and can provide extremely valuable insights into the constraints and oppor- tunities that govern evolution. In particular, comparing the genetic determinants of the independent origins of an adap- tive phenotype can shed new light on the role of genomic background in restricting or opening new evolutionary tra- jectories towards adaptive innovations [18–22]. In this paper we discuss the potential causes of convergence at the genetic level together with their implications for our understanding of evolutionary biology in general. When phenotypic convergence is caused by mutations in the same gene In the numerous reports of phenotypic convergence the responsible genetic mechanisms remain largely unknown because their identification is often complicated by the involvement of complex biochemical cascades as well as epistatic interactions [19,23,24]. In some cases it has been shown that different loci are involved in phenotypic con- vergence (e.g. Refs [8,25,26]), demonstrating that similar phenotypes can be reached through alterations of distinct enzymes. However, other studies have traced phenotypic convergence to modifications of homologous genes (e.g. Refs [3,5,6,26,27]); in this paper such phenomena will be further referred to as convergent recruitment (Glossary). The independent involvement of homologous genes in the emergence of a given phenotype probably results from strongly biased potential for a given phenotypic change as a consequence of mutations in different genes [28,29]. In cases where the new phenotype repeatedly occurs through a loss of enzymatic function, such as albinism or the absence of specific pigments [7,12], alterations of genes encoding elements involved in the biochemical cascade that cause the trait of interest are more likely to lead to the new phenotype. Silencing mutations also have a higher probability of being fixed when they occur in genes that can block the entire biochemical cascade without major dele- terious pleiotropic effects on the organism. Therefore, genes involved in multiple functions are poor candidates for phenotype loss through gene silencing. However, repeated cis-regulatory changes involved in the recurrent loss (or gain) of organ-specific gene expression have been reported [30]. Such modifications allow silencing Opinion Glossary Convergence: independent appearance of the same trait in different lineages. Convergent recruitment: the process of homologous gene becoming recur- rently responsible for a novel function. Convergent substitution: replacement of the same ancestral character (e.g. amino acid) by an identical character. Epistatic interaction: influence of one gene on the expression of another gene. Gene family: a group of homologous genes which are generally responsible for similar catalytic reactions. Multigene families contain several gene lineages, and these usually fulfill different functions. Gene lineage: a gene family that arose via whole genome or gene duplication. Genes of the same lineage are orthologous, but more recent gene duplications can hamper the definition of orthology. Homology: the relationship between genes that share a common ancestor. This includes orthologs as well as paralogs. This term is restricted to genes whose relationship can be deduced from sequence similarity. Orthologs: genes in different species whose divergence is due to speciation. Paralogs: genes whose divergence is due to single gene or whole genome duplication. Phenotype: the observable characteristic that results from the expression of genes with the possibility of additional environmental effects. Phenotypes include organism traits as well as all measurable properties of enzymes. Pleiotropic effect: the action of a single gene on apparently unrelated phenotypic traits. Corresponding author: Christin, P.-A. (Pascal-Antoine_Christin@brown.edu) 400 0168-9525/$ – see front matter ß 2010 Elsevier Ltd. All rights reserved. doi:10.1016/j.tig.2010.06.005 Trends in Genetics 26 (2010) 400–405